Sorting of the yeast vacuolar-type, proton-translocating ATPase enzyme complex (V-ATPase): Identification of a necessary and sufficient Golgi/endosomal retention signal in Stv1p

Journal of Biological Chemistry

Volumn 287, Issue 23, 2012, Pages 19487-19500

  Finnigan, Gregory C ^a   Cronan, Glen E ^a   Park, Hae J ^a   Srinivasan, Sankaranarayanan ^b   Quiocho, Florante A ^b   Stevens, Tom H ^a  

^a UNIVERSITY OF OREGON   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSOLIC; ENDOSOMES; ENZYME COMPLEXES; HOMOLOGY MODELING; ISOFORMS; MEIOTHERMUS RUBER; MOLECULAR MACHINES; MUTANT ALLELES; N-TERMINALS; PEPTIDE SEQUENCES; PROTON TRANSLOCATION; RANDOM MUTAGENESIS; SORTING MACHINERY; SORTING SIGNALS; STRUCTURAL MODELS; SUBCELLULAR LOCALIZATIONS; V-ATPASE; VACUOLAR MEMBRANES;

ENZYMES; MACHINERY; MODEL STRUCTURES; PROTONS; THREE DIMENSIONAL; YEAST;

SORTING;

ISOENZYME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; STV1P PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOSOME; ENZYME LOCALIZATION; ENZYME SUBUNIT; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; MEIOTHERMUS RUBER; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; THERMUS; YEAST;

AMINO ACID MOTIFS; ENDOSOMES; EVOLUTION, MOLECULAR; ISOENZYMES; MODELS, MOLECULAR; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN; TRANS-GOLGI NETWORK; VACUOLAR PROTON-TRANSLOCATING ATPASES;

MEIOTHERMUS RUBER;

EID: 84861752198     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.343814     Document Type: Article

References (90)

1. Forgac, M. (2007) Vacuolar ATPases. Rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8, 917-929
2. Hirata, T., Iwamoto-Kihara, A., Sun-Wada, G. H., Okajima, T., Wada, Y., and Futai, M. (2003) Subunit rotation of vacuolar-type proton pumping ATPase. Relative rotation of the G and C subunits. J. Biol. Chem. 278, 23714-23719 (Pubitemid 36830195)
3. Yokoyama, K., Nakano, M., Imamura, H., Yoshida, M., and Tamakoshi, M. (2003) Rotation of the proteolipid ring in the V-ATPase. J. Biol. Chem. 278, 24255-24258 (Pubitemid 37548574)
4. +-ATPases. Nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 3, 94-103
5. Muench, S. P., Trinick, J., and Harrison, M. A. (2011) Structural divergence of the rotary ATPases. Q. Rev. Biophys. 44, 311-356
6. +-ATPase. J. Bioenerg. Biomembr. 39, 415-421
7. Hinton, A., Bond, S., and Forgac, M. (2009) V-ATPase functions in normal and disease processes. Pflugers Arch. 457, 589-598
8. +-ATPase is decreased in microvascular endothelial cells from a diabetic model. J. Cell Physiol. 201, 190-200
9. +-ATPase inhibitor bafilomycin A1 differentially affects proteolytic processing of mutant and wild-type β- amyloid precursor protein. J. Biol. Chem. 270, 6186-6192
10. Nishiguchi, M., Tokugawa, K., Yamamoto, K., Akama, T., Nozawa, Y., Chaki, S., Ueki, T., Kameo, K., and Okuyama, S. (2003) Increase in secretion of glial cell line-derived neurotrophic factor from glial cell lines by inhibitors of vacuolar ATPase. Neurochem. Int. 42, 493-498 (Pubitemid 36120652)
11. +-ATPase in human breast cancer cells with distinct metastatic potential: distribution and functional activity. Am. J. Physiol. Cell Physiol. 286, C1443-C1452
12. Goldstein, D. J., Finbow, M. E., Andresson, T., McLean, P., Smith, K., Bubb, V., and Schlegel, R. (1991) Bovine papillomavirus E5 oncoprotein binds to the 16K component of vacuolar H+-ATPases. Nature 352, 347-349 (Pubitemid 21912357)
13. +-ATPase activity by a Legionella pneumophila effector. PLoS Pathog. 6, e1000822
14. Pérez-Sayáns, M., Somoza-Martín, J. M., Barros-Angueira, F., Diz, P. G., Rey, J. M., and García-García, A. (2010) Multidrug resistance in oral squamous cell carcinoma. The role of vacuolar ATPases. Cancer Lett. 295, 135-143
15. +-ATPase subunits onto the vacuolar membrane in Saccharomyces cerevisiae. J. Biol. Chem. 268, 961-967
16. +- ATPase complex. J. Biol. Chem. 270, 22329-22336
17. Malkus, P., Graham, L. A., Stevens, T. H., and Schekman, R. (2004) Role of Vma21p in assembly and transport of the yeast vacuolar ATPase. Mol.Biol. Cell 15, 5075-5091 (Pubitemid 39392221)
18. Davis-Kaplan, S. R., Compton, M. A., Flannery, A. R., Ward, D. M., Kaplan, J., Stevens, T. H., and Graham, L. A. (2006) PKR1 encodes an assembly factor for the yeast V-type ATPase. J. Biol. Chem. 281, 32025-32035 (Pubitemid 46041463)
19. Ryan, M., Graham, L. A., and Stevens, T. H. (2008) Voa1p functions in V-ATPase assembly in the yeast endoplasmic reticulum. Mol. Biol. Cell 19, 5131-5142
20. +-ATPase. Microbiol. Mol. Biol. Rev. 70, 177-191
21. Graham, L. A., Flannery, A. R., and Stevens, T. H. (2003) Structure and assembly of the yeast V-ATPase. J. Bioenerg. Biomembr. 35, 301-312 (Pubitemid 37288697)
22. Klionsky, D. J., Herman, P. K., and Emr, S. D. (1990) The fungal vacuole. Composition, function, and biogenesis. Microbiol. Rev. 54, 266-292
23. Finnigan, G. C., Hanson-Smith, V., Houser, B. D., Park, H. J., and Stevens, T. H. (2011) The reconstructed ancestral subunit a functions as both VATPase isoforms Vph1p and Stv1p in Saccharomyces cerevisiae. Mol. Biol. Cell 22, 3176-3191
24. Leng, X. H., Nishi, T., and Forgac, M. (1999) Transmembrane topography of the 100-kDa a subunit (Vph1p) of the yeast vacuolar proton-translocating ATPase. J. Biol. Chem. 274, 14655-14661
25. 2 terminus of vph1p, an integral subunit of the V0 sector of the yeast V-ATPase, interacts directly with the Vma1p and Vma13p subunits of the V1 sector. J. Biol. Chem. 275, 15449-15457
26. Kawasaki-Nishi, S., Nishi, T., and Forgac, M. (2001) Arg-735 of the 100- kDa subunit a of the yeast V-ATPase is essential for proton translocation. Proc. Natl. Acad. Sci. U.S.A. 98, 12397-12402 (Pubitemid 33019957)
27. +-ATPase subunit Vph1p. J. Biol. Chem. 269, 14064-14074
28. Qi, J., and Forgac, M. (2007) Cellular environment is important in controlling V-ATPase dissociation and its dependence on activity. J. Biol. Chem. 282, 24743-24751 (Pubitemid 47347540)
29. +- ATPase. J. Biol. Chem. 267, 14294-14303
30. Leng, X. H., Manolson, M. F., and Forgac, M. (1998) Function of the COOH-terminal domain of Vph1p in activity and assembly of the yeast V-ATPase. J. Biol. Chem. 273, 6717-6723 (Pubitemid 28160331)
31. Kawasaki-Nishi, S., Nishi, T., and Forgac, M. (2001) Yeast V-ATPase complexes containing different isoforms of the 100-kDa a-subunit differ in coupling efficiency and in vivo dissociation. J. Biol. Chem. 276, 17941-17948
32. Perzov, N., Padler-Karavani, V., Nelson, H., and Nelson, N. (2002) Characterization of yeast V- ATPase mutants lacking Vph1p or Stv1p and the effect on endocytosis. J. Exp. Biol. 205, 1209-1219 (Pubitemid 34853757)
33. Kawasaki-Nishi, S., Bowers, K., Nishi, T., Forgac, M., and Stevens, T. H. (2001) The amino-terminal domain of the vacuolar proton-translocating ATPase a subunit controls targeting and in vivo dissociation, and the carboxyl-terminal domain affects coupling of proton transport and ATP hydrolysis. J. Biol. Chem. 276, 47411-47420
34. Collins, B. M. (2008) The structure and function of the retromer protein complex. Traffic 9, 1811-1822
35. Bonifacino, J. S., and Hurley, J. H. (2008) Retromer. Curr. Opin. Cell Biol. 20, 427-436
36. +-ATPase in vesicular trafficking. Targeting, regulation, and function. Curr. Opin. Cell Biol. 20, 415-426
37. +-ATPase subunit a. J. Biol. Chem. 276, 40050-40054
38. +-ATPase. Cell- specific expression during development. J. Biol. Chem. 276, 33079-33085
39. +-ATPase with the a3 isoform during osteoclast differentiation. J. Biol. Chem. 278, 22023-22030
40. Wassmer, T., Kissmehl, R., Cohen, J., and Plattner, H. (2006) Seventeen a-subunit isoforms of paramecium V-ATPase provide high specialization in localization and function. Mol. Biol. Cell 17, 917-930 (Pubitemid 43191124)
41. +-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18, 715-730
42. Smith, A. N., Skaug, J., Choate, K. A., Nayir, A., Bakkaloglu, A., Ozen, S., Hulton, S. A., Sanjad, S. A., Al-Sabban, E. A., Lifton, R. P., Scherer, S. W., and Karet, F. E. (2000) Mutations in ATP6N1B, encoding a new kidney vacuolar proton pump 116-kDa subunit, cause recessive distal renal tubular acidosis with preserved hearing. Nat. Genet. 26, 71-75
43. Frattini, A., Orchard, P. J., Sobacchi, C., Giliani, S., Abinun, M., Mattsson, J. P., Keeling, D. J., Andersson, A. K., Wallbrandt, P., Zecca, L., Notarangelo, L. D., Vezzoni, P., and Villa, A. (2000) Defects in TCIRG1 subunit of the vacuolar proton pump are responsible for a subset of human autosomal recessive osteopetrosis. Nat. Genet. 25, 343-346 (Pubitemid 30437326)
44. Schekman, R., and Orci, L. (1996) Coat proteins and vesicle budding. Science 271, 1526-1533 (Pubitemid 26097211)
45. Nothwehr, S. F., Roberts, C. J., and Stevens, T. H. (1993) Membrane protein retention in the yeast Golgi apparatus. Dipeptidyl aminopeptidase A is retained by a cytoplasmic signal containing aromatic residues. J. Cell Biol. 121, 1197-1209 (Pubitemid 23174539)
46. Sandoval, I. V., and Bakke O. (1994) Targeting of membrane proteins to endosomes and lysosomes. Trends Cell Biol. 4, 292-297 (Pubitemid 24223532)
47. Ohno, H., Stewart, J., Fournier, M. C., Bosshart, H., Rhee, I., Miyatake, S., Saito, T., Gallusser, A., Kirchhausen, T., and Bonifacino, J. S. (1995) Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269, 1872-1875
48. Mellman, I. (1996) Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 12, 575-625
49. Vowels, J. J., and Payne, G. S. (1998) A dileucine-like sorting signal directs transport into an AP-3-dependent, clathrin-independent pathway to the yeast vacuole. EMBO J. 17, 2482-2493 (Pubitemid 28221184)
50. Misra, S., Puertollano, R., Kato, Y., Bonifacino, J. S., and Hurley, J. H. (2002) Structural basis for acidic cluster-dileucine sorting signal recognition by VHS domains. Nature 415, 933-937 (Pubitemid 34174758)
51. Bonifacino, J. S., and Traub, L. M. (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72, 395-447 (Pubitemid 36930451)
52. Johnston, H. D., Foote, C., Santeford, A., and Nothwehr, S. F. (2005) Golgito- late endosome trafficking of the yeast pheromone processing enzyme Ste13p is regulated by a phosphorylation site in its cytosolic domain. Mol. Biol. Cell 16, 1456-1468 (Pubitemid 40349579)
53. Bryant, N. J., and Stevens, T. H. (1997) Two separate signals act independently to localize a yeast late Golgi membrane protein through a combination of retrieval and retention. J. Cell Biol. 136, 287-297 (Pubitemid 27063079)
54. Sambrook, J., and Russell, D. W. (2001) Molecular Cloning: A Laboratory Manual, 3rd Ed., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
55. Rothman, J. H., and Stevens, T. H. (1986) Protein sorting in yeast. Mutants defective in vacuole biogenesis mislocalize vacuolar proteins into the late secretory pathway. Cell 47, 1041-1051 (Pubitemid 17005076)
56. Goldstein, A. L., and McCusker, J. H. (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15, 1541-1553 (Pubitemid 29472165)
57. Zheng, L., Baumann, U., and Reymond, J. L. (2004) An efficient one-step site-directed and site saturation mutagenesis protocol. Nucleic Acids Res. 32, e115
58. Markwell, M. A., Haas, S. M., Bieber, L. L., and Tolbert, N. E. (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87, 206-210 (Pubitemid 9050428)
59. Srinivasan, S., Vyas, N. K., Baker, M. L., and Quiocho, F. A. (2011) Crystal structure of the cytoplasmic N-terminal domain of subunit I, a homolog of subunit a, of V-ATPase. J. Mol. Biol. 412, 14-21
60. Zhang, Y. (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9, 40
61. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) ClustalW and ClustalX version 2.0. Bioinformatics 23, 2947-2948
62. Sagermann, M., Stevens, T. H., and Matthews, B. W. (2001) Crystal structure of the regulatory subunit H of the V-type ATPase of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 98, 7134-7139 (Pubitemid 32567915)
63. Drory, O., Frolow, F., and Nelson, N. (2004) Crystal structure of yeast V-ATPase subunit C reveals its stator function. EMBO Rep. 5, 1148-1152 (Pubitemid 40103608)
64. Diepholz, M., Venzke, D., Prinz, S., Batisse, C., Flörchinger, B., Rössle, M., Svergun, D. I., Böttcher, B., and Féthière, J. (2008) A different conformation for EGC stator subcomplex in solution and in the assembled yeast V-ATPase. Possible implications for regulatory disassembly. Structure 16, 1789-1798
65. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera.Avisualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
66. 2+ levels in S. cerevisiae. FEBS Lett. 451, 132-136
67. MacDiarmid, C. W., Gaither, L. A., and Eide, D. (2000) Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J. 19, 2845-2855 (Pubitemid 30386757)
68. Jo, W. J., Kim, J. H., Oh, E., Jaramillo, D., Holman, P., Loguinov, A. V., Arkin, A. P., Nislow, C., Giaever, G., and Vulpe, C. D. (2009) Novel insights into iron metabolism by integrating deletome and transcriptome analysis in an iron deficiency model of the yeast Saccharomyces cerevisiae. BMC Genomics 10, 130
69. Hill, K., and Cooper, A. A. (2000) Degradation of unassembled Vph1p reveals novel aspects of the yeast ER quality control system. EMBO J. 19, 550-561 (Pubitemid 30093728)
70. Thompson, J. D., Higgins, D. G., Gibson, T. J. (1994) ClustalW. Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 (Pubitemid 24354800)
71. Cowles, C. R., Odorizzi, G., Payne, G. S., and Emr, S. D. (1997) The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 91, 109-118 (Pubitemid 27431317)
72. Piper, R. C., Bryant, N. J., and Stevens, T. H. (1997) The membrane protein alkaline phosphatase is delivered to the vacuole by a route that is distinct from the VPS-dependent pathway. J. Cell Biol. 138, 531-545 (Pubitemid 27349836)
73. Stepp, J. D., Huang, K., and Lemmon, S. K. (1997) The yeast adaptor protein complex, AP-3, is essential for the efficient delivery of alkaline phosphatase by the alternate pathway to the vacuole. J. Cell Biol. 139, 1761-1774 (Pubitemid 28079240)
74. Toei, M., Saum, R., and Forgac, M. (2010) Regulation and isoform function of the V-ATPases. Biochemistry 49, 4715-4723
75. Ediger, B., Melman, S. D., Pappas, D. L. Jr., Finch, M., Applen, J., and Parra, K. J. (2009) The tether connecting cytosolic (N terminus) and membrane (C terminus) domains of yeast V-ATPase subunit a (Vph1) is required for assembly of V0 subunit d. J. Biol. Chem. 284, 19522-19532
76. Otte, S., and Barlowe, C. (2002) The Erv41p-Erv46p complex. Multiple export signals are required in trans for COPII-dependent transport from the ER. EMBO J. 21, 6095-6104 (Pubitemid 35415326)
77. Oestreich, A. J., Aboian, M., Lee, J., Azmi, I., Payne, J., Issaka, R., Davies, B. A., and Katzmann, D. J. (2007) Characterization of multiple multivesicular body sorting determinants within Sna3. A role for the ubiquitin ligase Rsp5. Mol. Biol. Cell 18, 707-720 (Pubitemid 46213238)
78. Qi, J., and Forgac, M. (2008) Function and subunit interactions of the N-terminal domain of subunit a (Vph1p) of the yeast V-ATPase. J. Biol. Chem. 283, 19274-19282
79. Kawasaki-Nishi, S., Nishi, T., and Forgac, M. (2003) Interacting helical surfaces of the transmembrane segments of subunits a and c′ of the yeast V-ATPase defined by disulfide-mediated cross-linking. J. Biol. Chem. 278, 41908-41913 (Pubitemid 37310452)
80. Wang, Y., Inoue, T., and Forgac, M. (2004) TM2 but not TM4 of subunit c″interacts with TM7 of subunit a of the yeast V-ATPase as defined by disulfide-mediated cross-linking. J. Biol. Chem. 279, 44628-44638 (Pubitemid 39430871)
81. Harms, M. J., and Thornton, J. W. (2010) Analyzing protein structure and function using ancestral gene reconstruction. Curr. Opin. Struct. Biol. 20, 360-366
82. Thornton, J. W. (2004) Resurrecting ancient genes. Experimental analysis of extinct molecules. Nat. Rev. Genet. 5, 366-375
83. Dean, A. M., and Thornton, J. W. (2007) Mechanistic approaches to the study of evolution. The functional synthesis. Nat. Rev. Genet. 8, 675-688 (Pubitemid 47281989)
84. Nothwehr, S. F., Bruinsma, P., and Strawn, L. A. (1999) Distinct domains within Vps35p mediate the retrieval of two different cargo proteins from the yeast prevacuolar/endosomal compartment. Mol. Biol. Cell 10, 875-890 (Pubitemid 29193718)
85. Nothwehr, S. F., Ha, S. A., and Bruinsma, P. (2000) Sorting of yeast membrane proteins into an endosome-to-Golgi pathway involves direct interaction of their cytosolic domains with Vps35p. J. Cell Biol. 151, 297-310
86. Arighi, C. N., Hartnell, L. M., Aguilar, R. C., Haft, C. R., and Bonifacino, J. S. (2004) Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 165, 123-133 (Pubitemid 38649182)
87. Seaman, M. N. (2007) Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J. Cell Sci. 120, 2378-2389
88. Canuel, M., Lefrancois, S., Zeng, J., and Morales, C. R. (2008) AP-1 and retromer play opposite roles in the trafficking of sortilin between the Golgi apparatus and the lysosomes. Biochem. Biophys. Res. Commun. 366, 724-730
89. Cooper, A. A., and Stevens, T. H. (1996) Vps10p cycles between the late Golgi and prevacuolar compartments in its function as the sorting receptor for multiple yeast vacuolar hydrolases. J. Cell Biol. 133, 529-541 (Pubitemid 26160966)
90. Strochlic, T. I., Setty, T. G., Sitaram, A., and Burd, C. G. (2007) Grd19/ Snx3p functions as a cargo-specific adapter for retromer-dependent endocytic recycling. J. Cell Biol. 177, 115-125 (Pubitemid 46588406)